Constitutively active Notch1 signaling promotes endothelial-mesenchymal transition in a conditional transgenic mouse model

International Journal of Molecular Medicine

Volumn 34, Issue 3, 2014, Pages 669-676

  Liu, Ju ^a,b,c   Dong, Fengyun ^a   Jeong, James ^b   Masuda, Takahiro ^b   Lobe, Corrinne G ^b,c  

^a SHANDONG UNIVERSITY   (China)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Cre loxP; Endothelial mesenchymal transition; Notch; Snail; Transgenic mice

Indexed keywords

ALKALINE PHOSPHATASE; ALPHA SMOOTH MUSCLE ACTIN; ANGIOPOIETIN RECEPTOR; CD31 ANTIGEN; CRE RECOMBINASE; EPHRIN B2; NOTCH1 RECEPTOR; TRANSCRIPTION FACTOR SNAIL; VASCULAR ENDOTHELIAL CADHERIN; INTEGRASE; SNAIL FAMILY TRANSCRIPTION FACTORS; TRANSCRIPTION FACTOR;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; EMBRYO; ENDOTHELIUM CELL; EPITHELIAL MESENCHYMAL TRANSITION; HEART DEVELOPMENT; MESENCHYME CELL; MOUSE; MOUSE EMBRYO; MOUSE MODEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; UPREGULATION; VASCULARIZATION; YOLK SAC; ANIMAL; ANIMAL EMBRYO; ANIMAL MODEL; CHEMISTRY; CYTOLOGY; EMBRYOLOGY; ENDOTHELIUM; HEART; HUMAN; MESODERM; METABOLISM; PROTEIN TERTIARY STRUCTURE;

ANIMALS; EMBRYO, MAMMALIAN; ENDOTHELIUM; EPHRIN-B2; HEART; HUMANS; INTEGRASES; MESODERM; MICE, TRANSGENIC; MODELS, ANIMAL; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, NOTCH1; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTORS;

EID: 84905055450     PISSN: 11073756     EISSN: 1791244X     Source Type: Journal    
DOI: 10.3892/ijmm.2014.1818     Document Type: Article

References (60)

1. Kovacic JC, Mercader N, Torres M, Boehm M and Fuster V: Epithelial-to-mesenchymal and endothelial-to-mesenchymal transition: from cardiovascular development to disease. Circulation 125: 1795-1808, 2012.
2. Zeisberg EM, Tarnavski O, Zeisberg M, et al: Endothelial-to-mesenchymal transition contributes to cardiac fibrosis. Nat Med 13: 952-961, 2007.
3. Garcia J, Sandi MJ, Cordelier P, et al: Tie1 deficiency induces endothelial-mesenchymal transition. EMBO Rep 13: 431-439, 2012.
4. Arciniegas E, Neves CY, Carrillo LM, Zambrano EA and Ramírez R: Endothelial-mesenchymal transition occurs during embryonic pulmonary artery development. Endothelium 12: 193-200, 2005.
5. Markwald RR, Fitzharris TP and Smith WN: Structural analysis of endocardial cytodifferentiation. Dev Biol 42: 160-180, 1975.
6. Markwald RR, Fitzharris TP and Manasek FJ: Structural development of endocardial cushions. Am J Anat 148: 85-119, 1977.
7. Arciniegas E, Frid MG, Douglas IS and Stenmark KR: Perspectives on endothelial-to-mesenchymal transition: potential contribution to vascular remodeling in chronic pulmonary hypertension. Am J Physiol 293: L1-L8, 2007.
8. Li J and Bertram JF: Review: Endothelial-myofibroblast transition, a new player in diabetic renal fibrosis. Nephrology (Carlton) 15: 507-512, 2010.
9. Xu H, Zaidi M, Struve J, et al: Abnormal fibrillin-1 expression and chronic oxidative stress mediate endothelial mesenchymal transition in a murine model of systemic sclerosis. Am J Physiol Cell Physiol 300: C550-C556, 2011.
10. Kizu A, Medici D and Kalluri R: Endothelial-mesenchymal transition as a novel mechanism for generating myofibroblasts during diabetic nephropathy. Am J Pathol 175: 1371-1373, 2009.
11. Yoshimatsu Y and Watabe T: Roles of TGF-β signals in endothelial-mesenchymal transition during cardiac fibrosis. Int J Inflam 2011: 724080, 2011.
12. Armstrong EJ and Bischoff J: Heart valve development: endothelial cell signaling and differentiation. Circ Res 95: 459-470, 2004.
13. High FA, Jain R, Stoller JZ, et al: Murine Jagged1/Notch signaling in the second heart field orchestrates Fgf8 expression and tissue-tissue interactions during outflow tract development. J Clin Invest 119: 1986-1996, 2009.
14. Garside VC, Chang AC, Karsan A and Hoodless PA: Co-ordinating Notch, BMP, and TGF-β signaling during heart valve development. Cell Mol Life Sci 70: 2899-2917, 2013.
15. Fu Y, Chang A, Chang L, et al: Differential regulation of transforming growth factor beta signaling pathways by Notch in human endothelial cells. J Biol Chem 284: 19452-19462, 2009.
16. Lewis J: Notch signalling. A short cut to the nucleus. Nature 393: 304-305, 1998.
17. Gridley T: Notch signaling in vascular development and physio logy. Development 134: 2709-2718, 2007.
18. Gridley T: Notch signaling during vascular development. Proc Natl Acad Sci USA 98: 5377-5378, 2001.
19. Fortini ME and Artavanis-Tsakonas S: The suppressor of hairless protein participates in notch receptor signaling. Cell 79: 273-282, 1994.
20. Tun T, Hamaguchi Y, Matsunami N, Furukawa T, Honjo T and Kawaichi M: Recognition sequence of a highly conserved DNA binding protein RBP-J kappa. Nucleic Acids Res 22: 965-971, 1994.
21. Krebs LT, Xue Y, Norton CR, et al: Notch signaling is essential for vascular morphogenesis in mice. Genes Dev 14: 1343-1352, 2000.
22. Noseda M, McLean G, Niessen K, et al: Notch activation results in phenotypic and functional changes consistent with endothelial-to-mesenchymal transformation. Circ Res 94: 910-917, 2004.
23. Grieskamp T, Rudat C, Lüdtke TH, Norden J and Kispert A: Notch signaling regulates smooth muscle differentiation of epicardium-derived cells. Circ Res 108: 813-823, 2011.
24. Chang AC, Fu Y, Garside VC, et al: Notch initiates the endothelial-to-mesenchymal transition in the atrioventricular canal through autocrine activation of soluble guanylyl cyclase. Dev Cell 21: 288-300, 2011.
25. Noseda M, Fu Y, Niessen K, et al: Smooth muscle alpha-actin is a direct target of Notch/CSL. Circ Res 98: 1468-1470, 2006.
26. Penton AL, Leonard LD and Spinner NB: Notch signaling in human development and disease. Semin Cell Dev Biol 23: 450-457, 2012.
27. Duarte A, Hirashima M, Benedito R, et al: Dosage-sensitive requirement for mouse Dll4 in artery development. Genes Dev 18: 2474-2478, 2004.
28. Krebs LT, Shutter JR, Tanigaki K, Honjo T, Stark KL and Gridley T: Haploinsufficient lethality and formation of arteriovenous malformations in Notch pathway mutants. Genes Dev 18: 2469-2473, 2004.
29. Xue Y, Gao X, Lindsell CE, et al: Embryonic lethality and vascular defects in mice lacking the Notch ligand Jagged1. Hum Mol Genet 8: 723-730, 1999.
30. Liu J and Lobe CG: Cre-conditional expression of constitutively active Notch1 in transgenic mice. Genesis 45: 259-265, 2007.
31. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA and Yanagisawa M: Tie2-Cre transgenic mice: a new model for endothelial cell-lineage analysis in vivo. Dev Biol 230: 230-242, 2001.
32. Lobe CG, Koop KE, Kreppner W, Lomeli H, Gertsenstein M and Nagy A: Z/AP, a double reporter for cre-mediated recombination. Dev Biol 208: 281-292, 1999.
33. Liu J, Kanki Y, Okada Y, et al: A +220 GATA motif mediates basal but not endotoxin-repressible expression of the von Willebrand factor promoter in Hprt-targeted transgenic mice. J Thromb Haemost 7: 1384-1392, 2009.
34. Baldwin HS, Shen HM, Yan HC, et al: Platelet endothelial cell adhesion molecule-1 (PECAM-1/CD31): alternatively spliced, functionally distinct isoforms expressed during mammalian cardiovascular development. Development 120: 2539-2553, 1994.
35. Eisenberg LM and Markwald RR: Molecular regulation of atrioventricular valvuloseptal morphogenesis. Circ Res 77: 1-6, 1995.
36. Nieto MA, Sargent MG, Wilkinson DG and Cooke J: Control of cell behavior during vertebrate development by Slug, a zinc finger gene. Science 264: 835-839, 1994.
37. Bolós V, Peinado H, Pérez-Moreno MA, Fraga MF, Esteller M and Cano A: The transcription factor Slug represses E-cadherin expression and induces epithelial to mesenchymal transitions: a comparison with Snail and E47 repressors. J Cell Sci 116: 499-511, 2003.
38. Adams RH, Wilkinson GA, Weiss C, et al: Roles of ephrinB ligands and EphB receptors in cardiovascular development: demarcation of arterial/venous domains, vascular morphogenesis, and sprouting angiogenesis. Genes Dev 13: 295-306, 1999.
39. Gerety SS and Anderson DJ: Cardiovascular ephrinB2 function is essential for embryonic angiogenesis. Development 129: 1397-1410, 2002.
40. Niessen K and Karsan A: Notch signaling in the developing cardiovascular system. Am J Physiol 293: C1-C11, 2007.
41. Carmeliet P: Mechanisms of angiogenesis and arteriogenesis. Nat Med 6: 389-395, 2000.
42. Risau W: Mechanisms of angiogenesis. Nature 386: 671-674, 1997.
43. Fischer A, Schumacher N, Maier M, Sendtner M and Gessler M: The Notch target genes Hey1 and Hey2 are required for embryonic vascular development. Genes Dev 18: 901-911, 2004.
44. Uyttendaele H, Ho J, Rossant J and Kitajewski J: Vascular patterning defects associated with expression of activated Notch4 in embryonic endothelium. Proc Natl Acad Sci USA 98: 5643-5648, 2001.
45. Kang Y and Massague J: Epithelial-mesenchymal transitions: twist in development and metastasis. Cell 118: 277-279, 2004.
46. Iso T, Hamamori Y and Kedes L: Notch signaling in vascular development. Arterioscler Thromb Vasc Biol 23: 543-553, 2003.
47. Garg V, Muth AN, Ransom JF, et al: Mutations in NOTCH1 cause aortic valve disease. Nature 437: 270-274, 2005.
48. Eldadah ZA, Hamosh A, Biery NJ, et al: Familial tetralogy of fallot caused by mutation in the jagged1 gene. Hum Mol Genet 10: 163-169, 2001.
49. Li L, Krantz ID, Deng Y, et al: Alagille syndrome is caused by mutations in human Jagged1, which encodes a ligand for Notch1. Nat Genet 16: 243-251, 1997.
50. Oka C, Nakano T, Wakeham A, et al: Disruption of the mouse RBP-J kappa gene results in early embryonic death. Development 121: 3291-3301, 1995.
51. Timmerman LA, Grego-Bessa J, Raya A, et al: Notch promotes epithelial-mesenchymal transition during cardiac development and oncogenic transformation. Genes Dev 18: 99-115, 2004.
52. Donovan J, Kordylewska A, Jan YN and Utset MF: Tetralogy of fallot and other congenital heart defects in Hey2 mutant mice. Curr Biol 12: 1605-1610, 2002.
53. Nieto MA: The snail superfamily of zinc-finger transcription factors. Nat Rev Mol Cell Biol 3: 155-166, 2002.
54. Murray SA and Gridley T: Snail family genes are required for left-right asymmetry determination, but not neural crest formation, in mice. Proc Natl Acad Sci USA 103: 10300-10304, 2006.
55. Vestweber D: VE-cadherin: the major endothelial adhesion molecule controlling cellular junctions and blood vessel formation. Arterioscler Thromb Vasc Biol 28: 223-232, 2008.
56. Lamouille S, Xu J and Derynck R: Molecular mechanisms of epithelial-mesenchymal transition. Nat Rev Mol Cell Biol 15: 178-196, 2014.
57. Cheng JC, Chang HM and Leung PC: Transforming growth factor-β1 inhibits trophoblast cell invasion by inducing Snail-mediated down-regulation of vascular endothelial-cadherin protein. J Biol Chem 288: 33181-33192, 2013.
58. Pérez-Pomares JM and de la Pompa JL: Signaling during epicardium and coronary vessel development. Circ Res 109: 1429-1442, 2011.
59. del Monte G, Casanova JC, Guadix JA, et al: Differential Notch signaling in the epicardium is required for cardiac inflow development and coronary vessel morphogenesis. Circ Res 108: 824-836, 2011.
60. Iso T, Maeno T, Oike Y, et al: Dll4-selective Notch signaling induces ephrinB2 gene expression in endothelial cells. Biochem Biophys Res Commun 341: 708-714, 2006.